Title

Neurovascular networks in epilepsy: Correlating ictal blood perfusion with intracranial electrophysiology

Authors

Balu Krishnan, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA. Electronic address: krishnb@ccf.org.
Simon Tousseyn, Academic Center for Epileptology, Kempenhaeghe and Maastricht UMC+, Heeze, The Netherlands.
Chetan Sateesh Nayak, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Thandar Aung, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Ammar Kheder, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Z Irene Wang, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Guiyun Wu, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Jorge Gonzalez-Martinez, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Dileep Nair, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Richard Burgess, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Leonidas Iasemidis, Center for Biomedical Engineering and Rehabilitation Science, Louisiana Tech University, Ruston, LA, USA.
Imad Najm, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Juan Bulacio, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.
Andreas V. Alexopoulos, Neurological Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, S51, Cleveland, OH 44195, USA.

Document Type

Article

Abstract

Perfusion patterns observed in Subtraction Ictal SPECT Co-registered to MRI (SISCOM) assist in focus localization and surgical planning for patients with medically intractable focal epilepsy. While the localizing value of SISCOM has been widely investigated, its relationship to the underlying electrophysiology has not been extensively studied and is therefore not well understood. In the present study, we set to investigate this relationship in a cohort of 70 consecutive patients who underwent ictal and interictal SPECT studies and subsequent stereo-electroencephalography (SEEG) monitoring for localization of the epileptogenic focus and surgical intervention. Seizures recorded during SEEG evaluation (SEEG seizures) were matched to semiologically-similar seizures during the preoperative ictal SPECT evaluation (SPECT seizures) by comparing the semiological changes in the course of each seizure. The spectral changes of the ictal SEEG with respect to interictal ones over 7 traditional frequency bands (0.1 to 150Hz) were analyzed at each SEEG site. Neurovascular (SEEG/SPECT) relations were assessed by comparing the estimated spectral power density changes of the SEEG at each site with the perfusion changes (SISCOM z-scores) estimated from the acquired SISCOM map at that site. Across patients, a significant correlation (p<0.05) was observed between spectral changes during the SEEG seizure and SISCOM perfusion z-scores. Brain sites with high perfusion z-score exhibited higher increased SEEG power in theta to ripple frequency bands with concurrent suppression in delta and theta frequency bands compared to regions with lower perfusion z-score. The dynamics of the correlation of SISCOM perfusion and SEEG spectral power from ictal onset to seizure end and immediate postictal period were also derived. Forty-six (46) of the 70 patients underwent resective epilepsy surgery. SISCOM z-score and power increase in beta to ripple frequency bands were significantly higher in resected than non-resected sites in the patients who were seizure-free following surgery. This study provides for the first time concrete evidence that both hyper-perfusion and hypo-perfusion patterns observed in SISCOM maps have strong electrophysiological underpinnings, and that integration of the information from SISCOM and SEEG can shed light on the location and dynamics of the underlying epileptic brain networks, and thus advance our anatomo-electro-clinical understanding and approaches to targeted diagnostic and therapeutic interventions.

Keywords

Epilepsy, Neurovascular Coupling, surgical outcome, SISCOM, Seizures, Stereo-encephalography

Medical Subject Headings

Adolescent; Adult; Brain (metabolism, physiopathology, surgery); Cerebrovascular Circulation (physiology); Child; Drug Resistant Epilepsy (metabolism, physiopathology, surgery); Electrocorticography (methods); Female; Humans; Male; Middle Aged; Nerve Net (metabolism, physiopathology, surgery); Neurovascular Coupling (physiology); Retrospective Studies; Spectroscopy, Near-Infrared (methods); Stereotaxic Techniques; Tomography, Emission-Computed, Single-Photon (methods); Young Adult

Publication Date

5-1-2021

Publication Title

NeuroImage

E-ISSN

1095-9572

Volume

231

First Page

117838

PubMed ID

33577938

Digital Object Identifier (DOI)

10.1016/j.neuroimage.2021.117838

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